ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on October 25, 2006
ICES Journal of Marine Science: Journal du Conseil 2007 64(1):141-148; doi:10.1093/icesjms/fsl012
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Age, growth, and reproduction of the roughskin skate, Dipturus trachyderma, from the southeastern Pacific
1 Universidad de Concepción, Facultad de Ciencias Naturales y Oceanográficas, Barrio Universitario s/n, Cabina 10, PO Box 160-C, Concepción, Chile
2 Instituto de Fomento Pesquero, Blanco 839, Valparaíso, Chile
Correspondence to R. Licandeo: tel: +56 41 2207029; fax: +56 41 2256571; e-mail: rlicandeo{at}hotmail.com
Licandeo, R., Cerna, F., and Céspedes, R. 2007. Age, growth, and reproduction of the roughskin skate, Dipturus trachyderma, from the southeastern Pacific. ICES Journal of Marine Science, 64: 141–148.Age, growth, and reproductive parameters of the roughskin skate, Dipturus trachyderma, in the southeastern Pacific are reported. Age was estimated by counting the growth rings of thin sections of vertebral centra from 201 fish (61–253 cm total length, LT). No systematic ageing bias was observed, and the precision of growth ring counts indicated a high level of reproducibility. Marginal increment analysis supported the hypothesis of annual deposition of growth rings, which form during winter. The oldest female and male were 26 and 25 y, respectively. Von Bertalanffy parameters for combined sexes based on length-at-age data were L
=257.7 cm LT, K=0.081 y–1 and t0=–1.363 y. Skates from the southernmost areas attained a larger mean size than those from more northern areas, and females reached a larger adult size than males. Males began the maturation process at 
186 cm LT, indicated by the abrupt enlargement of the claspers. Developed oviducal glands, uteri, and ovaries indicated that females began to mature at 200 cm LT. The length and age at which 50% of the population matured were 215 cm LT and 17 y for females and 195 cm LT and 15 y for males. The youngest mature female and male D. trachyderma were 15 and 13 y, respectively. The ovarian fecundity ranged from 28 to 68 follicles. Females carrying egg cases were found in March and July. Dipturus trachyderma is slow-growing, long-lived, attains large size, matures late, and has low fecundity, life history characteristics that make it highly susceptible to exploitation.
Keywords: age, Dipturus, growth, life history, maturity, reproduction, skates, South America
Received 23 February 2006; accepted 4 September 2006; advance access publication 25 October 2006.
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Introduction |
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Recent information has indicated the importance to management of species-specific data on skates, because catch-aggregated reports in landing statistics can mask significant changes in community structure and hide profound reductions in populations of large, slow-growing, late-maturing skates (Agnew et al., 2000; Dulvy et al., 2000). As a result of moderate to high levels of exploitation, common (Dipturus batis) and barndoor skates (D. laevis) have all but disappeared from substantial parts of their geographical ranges (Brander, 1981; Casey and Myers, 1998). Nevertheless, some smaller species have exhibited periods of population increase (Walker and Heessen, 1996; Agnew et al., 2000; Dulvy and Reynolds, 2002). Skate species that mature smaller or younger will have a greater likelihood of survival at high levels of exploitation because they are more likely to reproduce before being captured (Walker and Hislop, 1998).
The roughskin skate, D. trachyderma, is endemic to the temperate waters of South America. In the Pacific Ocean, it is found from Nugurue (36°08'S) to the Esteban Channel, in Chilean Patagonia (51°05'S) (Leible, 1987). In the Atlantic Ocean, the most recent records are from the central (Menni and Stehmann, 2000) and northeast San Jorge Gulf (46°S) (Cedrola et al., 2005). Dipturus trachyderma is caught together with a similar species, the kite skate (D. chilensis), which coexists throughout its distribution. However, D. trachyderma has been found in deeper waters on the continental shelf (200–400 m deep) than D. chilensis, which dominates over the continental shelf (Leible, 1987). The two species are targeted by artisanal longline fisheries in the waters of southern Chile. In the Atlantic Ocean off Argentine Patagonia, D. trachyderma has been recorded as bycatch in shrimp fisheries (Cedrola et al., 2005). Dipturus trachyderma attains larger size than D. chilensis, reaching a total length of 220 cm (Leible, 1987). However, the external morphology of the two species is similar, leading to frequent confusion between species. As a result, both species are placed in the same category and referred to collectively as "skates" in Chilean fisheries statistics.
Fisheries studies up to now have focused mainly on the most abundant species (Fuentealba and Leible, 1990; Gili et al., 1999; Licandeo et al., 2006), so no estimates of age or growth rates are currently available for D. trachyderma. Knowledge of its reproductive biology is also limited. With the exception of Leible (1987), who estimated length at maturity based on the development of claspers, no other aspects have been investigated. Adequate information on life history traits is key to understanding the ecology of the species and to implementing effective management and conservation measures. Therefore, we aim here to estimate for the first time life history traits of D. trachyderma, specifically age, growth rate, length–weight relationship, size and age at maturity, fecundity, and sex ratios.
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Material and methods |
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Sampling
The collection sites ranged from southern central Chile (39°45'S) to the Magellan Strait, in Chilean Patagonia (53°30'S). Specimens (33 females and 32 males) from southern central Chile (Figure 1) (Licandeo et al., 2006) were also collected during September and October 2001. Another 90 females and 101 males from the fjords and channels of southern Chile (Figure 1) were collected between the Seno de Reloncavi (41°28'S) and the Magellan Strait between September 2003 and September 2004. This area, unlike southern central Chile, contains large rivers and estuarine regions that are sheltered from exposed oceanic waters. All skates were caught with bottom longlines by artisanal fisheries.
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After capture, the following information was recorded for each skate: total length (LT, measured from the tip of the rostrum to the tip of the tail), disc width (WD, measured between the tips of the widest portions of the pectoral fins), pelvic length (LP, measured from the tip of the snout to the posterior margin of the pelvic fins), internal clasper length (LC, measured from the points of insertion at the cloaca to the tip of the claspers), and total mass (MT in kg). All measurements were recorded to the nearest 1 cm. As studies on skates often use WD or LP, the relationships between LT and both WD and LP were derived. A G-test (Sokal and Rohlf, 1995) was used to examine differences in the sex ratios. Log10-transformed length–weight relationships were calculated for each sex, then compared by analysis of covariance (ANCOVA), using Log10 LT as the covariate. A parallelism test was run before ANCOVA.
Age and growth
To estimate age, a section of 10 cm of the vertebral column consisting of approximately seven vertebrae from the area above the pelvic girdle was dissected from each specimen. The preparation of the vertebrae for enhancement, interpretation, and counting of growth rings was performed according to Licandeo et al. (2006). Vertebral sections were examined under a magnification of x20 using a dissecting microscope equipped with transmitted light. A growth ring was defined as a pair of bands, consisting of one highly calcified (opaque) band and one less-calcified (translucent) band. The analysis of thin sections of vertebrae was carried out by two readers. As a preliminary training exercise, the readers counted the growth rings on a subsample for discussion and interpretation. Subsequently, the two readers aged each skate independently without knowledge of its sex or size. Between-reader bias was determined from age–bias plots of band counts (Campana et al., 1995). Reproducibility of the growth ring count was evaluated with the coefficient of variation (CV) (Chang, 1982) and average per cent error (APE) (Beamish and Fournier, 1981).
The annual periodicity of growth ring deposition was investigated using marginal increment analysis (MIA), according to the following equation (Hayashi, 1976):
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Growth curves were fitted to length-at-age data using the von Bertalanffy growth model (VBGM) (von Bertalanffy, 1938). Model parameters were estimated using Marquardt's algorithm least-squares non-linear method. A likelihood ratio test was used to compare parameter estimates of the VBGM between sexes (Kimura, 1980; Haddon, 2001).
Reproductive data
The stages of maturity were defined according to previous studies on skates (Walmsley-Hart et al., 1999; Francis et al., 2001). In females, the juveniles had undeveloped sexual organs, with small ovaries and thread-like oviducts. Maturing females had slightly more enlarged ovaries, but without vitellogenic activity (pale colouration), forming translucent follicles of different sizes, and the oviducal glands and uterus can be differentiated from the oviducts. Mature active fish had fully developed ovaries, producing larger vitellogenic follicles that were easily identified by their yellow colouration. The oviducal glands were compact and kidney-shaped, and the uterus was extended and had the capacity to carry egg cases. Mature-postpartum fish had flaccid oviducal glands and uterus, indicating recent deposition of egg cases, and the ovaries had little or no vitellogenic activity. In males, the juveniles had small testes and small, flexible claspers that did not extend beyond the posterior edge of the pelvic fins. Maturing males had claspers that extended beyond the posterior edge of the pelvic fins, but the claspers remained soft and uncalcified. Mature males had large testes and coiled epididymis. The claspers were fully calcified and completely enlarged, and the clasper head (rhipidion) was rotated 90° relative to its normal position.
For females caught between September of 2003 and 2004, the reproductive organs were collected and analysed in the laboratory. The following data were recorded: weight of the two ovaries (g), width of the oviducal glands and the uterus, the ovarian fecundity (determined by counting the number of vitellogenic follicles), and if present, the width of the egg cases. All reproductive organs were measured to the nearest 0.1 mm with a vernier calliper. A paired sample t-test (Zar, 1984) was used to test for asymmetry between right and left reproductive organs.
Size and age at maturity
The size and age at which 50% of females and males attained maturity (L50% and A50%, respectively) was calculated by a logistic model for maximum likelihood procedures (Roa et al., 1999). This method utilizes binomial maturity data (immature=0, mature=1), so all females and males that were not capable of breeding (i.e. juveniles and maturing individuals) were grouped as immature.
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Results |
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In all, 256 specimens were collected. Females (n=123) ranged between 61 and 253 cm LT (mean±s.d.=174.7±44.68 cm) and 1.4–110.0 kg MT (n=110). Males (n=133) ranged between 59 and 232 cm LT (165.0±41.28 cm) and 3.0–66.0 kg MT (n=119). The relationships between LT and WD and between LT and LP were linear: LT=1.422WD–3.603 (r2=0.98, p<0.001, n=229) and LT=1.759LP–6.821 (r2=0.98, p<0.001, n=111). The length–weight relationships differed between sexes (F=7.979, d.f.=1 and 225, p=0.005), females attaining almost twice the adult weight of males (Figure 2). These relationships were described by the equations (without log10-transformation): females, MT=3.472E–03LT3.088 (r2=0.97, p<0.001, n=110); males, MT=2.368E–03LT3.150 (r2=0.98, p<0.001, n=118).
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The differences in observed size were significant between females and males caught from the southern–central and the fjords and channels of southern Chile (females, F=77.366, d.f.=1 and 121, p<0.001; males, F=136.249, d.f.=1 and 129, p<0.001). Dipturus trachyderma from the southern area attained a larger mean size (females, 202.7±31.37 cm LT; males, 196.5±23.87 cm LT) than those from the southern–central area (females, 147.1±38.31 cm LT; males, 138.9±31.63 cm LT). The ratio of males to females for each area did not differ significantly from a 1:1 ratio (southern–central, Gadj=6.16, p=0.432; southern Chile, Gadj=0.01, p=0.928).
Age and growth
Of the original 214 vertebral samples, vertebrae from 9 were taken from the caudal region, adjacent to the pelvic fins, where RV decreased sharply, so were not considered in order to avoid underestimation of age. The relationship between LT and vertebral radius (RV) was linear to 200 cm LT, then curvilinear for both females and males (Figure 3). Therefore, a quadratic model was preferred to describe the relationship. The equation for the combined sexes was LT=–208.528RV2+483.148RV–41.663 (r2=0.91, p<0.001, n=193).
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Growth bands along the intermedialia were usually indistinguishable owing to the interstitial spaces left by sectioning, so most band counts were derived from counts on the corpus calcareum. In general, no difficulty was encountered in estimating the age of D. trachyderma. However, identification of the last growth ring was more difficult in older fish, because the bands became closely spaced near the edge of the vertebrae. Four samples were unreadable. Age estimates agreed closely and there was no systematic bias between readers (Figure 4). The average IAPE of the overall sample was 3.52%, and the CV was 4.99. The levels of precision indicated a high level of reproducibility.
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Marginal increments were significantly different between months (H=23.028, groups=10, n=129, p=0.010) for samples corresponding to D. trachyderma with 2–15 growth rings. From February on (no data were available for January), the marginal increment decreased as the season progressed and was at its minimum during the months of June to August. It then increased from August, peaking during November and December. We therefore conclude that laying down of a growth ring begins in August and is completed in June, and that just one growth ring is formed annually (Figure 5).
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The oldest estimated age for a female D. trachyderma in this study was 26+ years (240 cm LT), whereas the age of the largest female was estimated to be 22 years (253 cm LT). For males, the oldest estimated age was 25+ years (212 cm LT), and the age of the largest male 23 years (225 cm LT). The overlap in observed size-at-age data indicated that the growth of both sexes did not differ up to the age of 16, when the fish reached a length of
210 cm. Thereafter, females continued growing to a larger size than males. However, a likelihood ratio test indicated that there was no difference in the VBGM between sexes (
2=5.699, d.f.=3, p=0.127), although females reached a larger L and had a lower K than males (Table 1). To allow for comparison with the literature, the growth parameters derived for sexes combined were used to describe the growth of the species (Figure 6, Table 1).
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Reproductive biology
The overall proportion of immature females, i.e. juveniles and maturing animals, differed markedly from mature females (1:2.05; Gadj=9.69, p=0.002). Examination of the reproductive tract revealed that there was no difference in the weight of the left and right ovaries (t=2.035, d.f.=33, p=0.105) or in the width of the oviducal glands (t=2.074, d.f.=22, p=0.889) or uterus (t=2,086, d.f.=20, p=0.886). Therefore, the mean was estimated and plotted against LT (Figure 7).
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Juveniles ranged in size from 61 to 160 cm LT, and maturing specimens from 123 to 207 cm LT. The pattern of enlargement of oviducal glands and uterus was characterized by them remaining undeveloped with a width <25 mm until the onset of maturity. At
200 cm LT, both oviducal glands and uterus began to enlarge, increasing sharply at 220 cm LT (Figure 7). In mature-active females (i.e. containing yellow follicles), the smallest specimen observed was 223 cm LT (67.0 kg; Figure 7). Mature-postpartum specimens ranged from 200 to 253 cm LT. The ovaries of those animals were reduced in size, and some were comparable in size to those of maturing skates. Additionally, some females had flaccid uteri and pale yellow follicles, likely indicating that a process of reabsorption had started. Only eight active females were found, all from late summer to early winter of 2004, in the fjords and channels of southern Chile. The ovaries contained light yellow follicles of different sizes, the largest follicle measuring 5.3 cm in diameter. The total ovary weight ranged from 887.0 to 1463.0 g (1185.8±311.90 g, n=4), and total ovarian fecundity from 28 to 68 follicles (48.7±12.18, n=7). Total ovary weight was significantly and positively correlated with total ovarian fecundity (r=0.88, t=3.244, p=0.048, n=5). Three females carrying one egg case per oviduct (single oviparity) were observed, one caught in late March and two in July 2004. The width of egg cases ranged from 150 to 157 mm. The smallest female found containing an egg case was 233 cm LT and 86.2 kg MT.
The overall proportion of immature males, i.e. juveniles and maturing skates, differed from mature males (1:1.65; Gadj=9.54, p=0.002). The claspers showed a noticeable change during the onset of maturity (Figure 8). Juveniles of 81–195 cm LT had short claspers measuring <16 cm. Most males began to mature at 186 cm LT, as indicated by the abrupt enlargement of the claspers, which increased to >40 cm LC. The largest maturing male was 209 cm LT and 25.5 cm LC, and the smallest mature male was 186 cm LT and 47 cm LC. All males >210 cm LT were fully mature, and the LC of these ranged from 43 to 57 cm.
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Size and age at maturity
Based on observations of 95 females (32.6% mature) and 109 males (37.6% mature), the L50% was estimated to be 215.0 cm LT for females and 195.1 cm LT for males (Figure 9a). The smallest mature female and male D. trachyderma were 200 and 183 cm LT, respectively. The A50% was estimated to be 17.4 y for females and 15.3 y for males (Figure 9b). The ages of the oldest immature female and male were 19 and 18 y, respectively, and the ages of the youngest mature female and male were 15 (210 cm LT) and 13 y (186 and 194 cm LT), respectively.
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Discussion |
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Skates from the southern area attained a greater size than those from the southern–central area. In areas farther north (36–41°S), Leible (1987) found that male D. trachyderma attained a maximum length of
200 cm, and females 220 cm LT. For Argentine Patagonia (42–48°S), Cedrola et al., (2005) recorded D. trachyderma males and females of up to 220 and 247 cm LT, respectively. In the current study, a male of 232 cm LT and a female of 253 cm LT were caught, both in the Smith Channel (52°S) in the southern area. Therefore, these data seem to indicate that there is an increase in LT with latitude in D. trachyderma. However, given that the number of samples was not sufficient to carry out analysis of life-history parameters by area, further studies would be needed to examine possible latitudinal variations in growth rates.
Age and growth
The relationship between LT and RV was curvilinear. This trend has also been observed in larger sharks such as Carcharhinus obscurus (Natanson et al., 1995), Lamna nasus (Natanson et al., 2002), and Prionace glauca (Skomal and Natanson, 2003). This could be the result of a decrease in growth rates of vertebrae as the animals reach maximum asymptotic size, and if so, could indicate that the largest D. trachyderma were effectively sampled and included in the analysis. In fact, the area studied covered a wide latitudinal area and a broad variety of environments, ranging from offshore to sheltered continental shelf waters.
Based on MIA, D. trachyderma appeared to form a single growth ring each year in late autumn or mid-winter. These results were similar to the tendency for marginal increments described for D. chilensis from southern–central Chile. Dipturus chilensis lays down growth rings during autumn and winter (Licandeo et al., 2006), but approximately a month later than D. trachyderma. Although the MIR analysis provided partial validation of the annual periodicity of growth rings in D. trachyderma, complete validation (for all age groups) is still required.
The likelihood ratio test did not show differences in the growth pattern of females and males. However, adult females were heavier and attained a larger L than males, and the growth completion rate, K, was higher in males than in females. We interpret this to indicate that adult females grow larger than adult males and that male growth rates tend to be faster, agreeing with previous reports for other rajid species (e.g. Walmsley-Hart et al., 1999; Licandeo et al., 2006).
Only three Dipturus species seem to reach sizes similar to those recorded for D. trachyderma: D. batis reach sizes of 250 cm LT (Walker and Hislop, 1998); D. innominatus attain at least 240 cm LT (Cox and Francis, 1997); and D. nidarosiensis reach 200 cm LT (Froese and Pauly, 2000). For larger species such as D. batis, Du Buit (1977) estimated that L=253.7 cm LT and that K=0.057 y–1, whereas Francis et al. (2001) estimated that L=150.5 cm LP and that K=0.095 y–1 for D. innominatus. The L estimated in this study (L=257.4 cm) is similar to that of D. batis. However, D. trachyderma had higher K values (K=0.081 y–1), more comparable to that of D. innominatus. On the other hand, estimates from vertebrae indicated that female D. trachyderma could live for at least 26 years. This estimated longevity is similar to that of female D. innominatus, which reach at least 24 y of age, and Du Buit (1977) estimated the maximum age of D. batis at 23 y. Therefore, D. trachyderma appears slow-growing and long-lived, exhibiting patterns comparable with those of other large species of Dipturus.
Reproductive biology
The pattern of maturity of D. trachyderma seems to be an abrupt process, as shown by a distinct development of reproductive organs relative to body size at the onset of maturity. Male D. trachyderma reach sexual maturity earlier than females. Females begin to mature at 200 cm LT, as indicated by the development of the uterus and the oviducal glands, whereas most males had fully developed claspers (i.e. were mature) at lengths of 186 cm LT. Similar estimates were given by Leible (1987) who, based on eight fish, estimated that male D. trachyderma attained maturity at 180 cm LT, as shown by enlargement of claspers from 25 to 50 cm.
Skates are usually capable of a prolonged season of egg-case deposition (Hamlett and Koob, 1999). According to those authors (1999), deep-water skates may deposit egg cases all year round, whereas shallow-water skates tend to have more seasonal patterns. Dipturus trachyderma is a deep-water species, found in waters up to 400 m deep (Leible, 1987), although they have also been caught between 87 and 97 m (Cedrola et al., 2005). Mature-active D. trachyderma (i.e. ovulating) were present in late summer (March) and early winter (July). However, given that few females carrying egg cases were found, more data are needed to identify the egg-deposition season for the species.
The fecundity ranged from 28 to 68 follicles, with an average of 49 follicles, an estimate similar to that reported by Fuentealba and Leible (1990) and Licandeo et al. (2006) for D. chilensis, in which ovarian fecundity ranged from 40 to 70 follicles. These estimates are similar to the maximum egg production for the related D. laevis, approximately 47 eggs (Casey and Myers, 1998).
Size and age at maturity
The estimates of age at maturity for both sexes are the highest that we could find described for any skate. Comparisons can be made with D. innominatus and D. batis, which reach similar size to D. trachyderma. Fifty per cent maturity of D. innominatus was estimated at 13 and 8 y, and 112 and 93 cm LP, for females and males, respectively (Francis et al., 2001). Using the relationship between LP and LT above, the L50% in LP of D. trachyderma corresponded to 127.6 and 115.8 cm LP for females and males, respectively. This indicates a pattern of very late maturity for the species. Unfortunately, only size at maturity of male D. batis is known, which is estimated at 125 cm LT or 11 years (Du Buit, 1977). From Figure 8 here, it is clear that there was no clasper development evident at 125 cm LT in D. trachyderma, whereas this size corresponds to the size at maturity documented for D. batis. Late maturity has also been estimated for D. chilensis; females do not reach 50% maturity until age 14 or 104 cm LT and males until 11 or 86 cm LT (Licandeo et al., 2006). Therefore, it appears that, in general, Dipturus species mature late.
Implications for fisheries management
Dipturus trachyderma was not abundant throughout the year, either in the fjords and channels or coastal waters within the sampling area. This supports observations made by Cedrola et al. (2005), based on D. trachyderma caught in the Southwest Atlantic from September 2001 to September 2002, where only 138 specimens was caught. In the current study, a similar number of skates was recorded during similar periods (n=191, September 2003–2004). Perhaps, its low abundance may reflect low productivity, some aspects of its life history presented here, e.g. late age at maturity, supporting this hypothesis. Smith et al. (1998), based on an analysis of 26 species of shark, stated that productivity was strongly influenced by age at maturity.
At present, it is difficult to develop a management plan for D. trachyderma owing to the lack of adequate information. For example, many aspects of the life history of D. trachyderma, such as stock structure, mortality, behaviour, spawning grounds, distribution, and movements, are still unknown. Moreover, there is at present only one management plan aimed at the skate fishery, the permitted maximum catch, but this does not discriminate between species.
Several studies have determined that the maximum size of rajid species is an indicator of low resilience to fishing pressure (Walker and Hislop, 1998; Stevens et al., 2000; Dulvy and Reynolds, 2002). In addition, Jennings et al. (1998), Dulvy et al. (2000), and Dulvy and Reynolds (2002) provided quantitative evidence that later-maturing, slower-growing, larger skates are more susceptible to decline when exploited. This could explain why populations of some larger members of the genus Dipturus have shown a significant decline over the past 20 years (Brander, 1981; Casey and Myers, 1998; Dulvy et al., 2000). Dipturus trachyderma is one of the largest skates in the Chilean skate community, and possibly one of the most susceptible to overexploitation. However, it is commonly confused with D. chilensis (Licandeo et al., 2006), and an overlap in ranges of similar species could have important implications for fisheries management, because the decline (or disappearance) of the most vulnerable species would not be detected. Therefore, we stress again the importance of identifying species accurately and conducting species-specific monitoring. Given the increasing fishing effort on stocks of skates in the fjords and channels of Chilean Patagonia and the slow life history of D. trachyderma, the species is clearly at risk, and conservation measures are urgently needed.
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Acknowledgements |
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We thank all fishers and scientific observers for their contributions, because without their contribution this paper would have not been possible. RL also thanks the owners of FV "Golondrina" for donating skate samples and for allowing us on board, Julio Lamilla (UACH) for support, and Pablo González (Antarctica Food) for encouragement. Mattias Braccini and an anonymous reviewer provided insightful comments that helped us to improve the manuscript. Finally, we thank Miguel Donoso (IFOP), José Perez (IFOP, Punta Arenas), and Marcelo García (SUBPESCA). The study was supported by the Fisheries Research Fund (FIP 2003–12).
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References |
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